In 1994, he portrayed convicted killer "Karl Mueller" in the Babylon 5 episode "The Quality of Mercy," as well as "Richard Odin," leader of a vegetarian cult in an episode of the X-Files called "Red Museum." He was also originally considered to voice the supervillain Firefly in Batman: The Animated Series in 1992, though the character was deemed unsuitable for the series and ultimately dropped. Rolston would later voice Firefly in the revamp, The New Batman Adventures, as well as Justice League. In 2004 Rolston would guest star in two episodes of the critically acclaimed 24.

He also appeared in a minor role in The CW series Supernatural in season 4 as the demon Alastair.

He had a voice-acting role in the video games Blade Runner (1997) and Turok (2008) and Halo 4 (2012). He also appeared in Criminal Minds in the episode, Blood Hungry as Sheriff Don Hall who asks for the BAU's help in finding out who's behind a series of violent murders.

He has a recurring role as Lex Luthor in the animated series Young Justice; his Shawshank Redemption co-star Clancy Brown also played Luthor for various animated TV shows over the course of his career.